implementing a regulatory budget: estimating the mandated private

ISSN 1330-0520 review paper / pregledni ~lanakUDK 598.112:591.128

FIELD BODY TEMPERATURES, MECHANISMSOF THERMOREGULATION AND EVOLUTION OF

THERMAL CHARACTERISTICS IN LACERTIDLIZARDS

AURORA M. CASTILLA1,2, RAOUL VAN DAMME1 & DIRK BAUWENS3

1Department of Biology, University of Antwerp (UIA),B–2610 Wilrijk, Belgium

2Instituto Mediterráneo de Estudios Avanzados,E–07071 Palma de Mallorca, Spain

3Institute of Nature Conservation, Kliniekstraat 25,B–1070 Brussel, Belgium

Castilla, A. M., Van Damme, R. & Bauwens, D.: Field body temperatures, mechanisms ofthermoregulation and evolution of thermal characteristics in lacertid lizards. Nat. Croat., Vol. 8,No. 3., 253–274, 1999, Zagreb.

We discuss three aspects of the thermal biology of lacertid lizards. First, we provide an over-view of the available data on field body temperatures (Tb), the thermal sensitivity of various per-formance functions and selected body temperatures in different species of lacertid lizards. We alsobriefly summarise information on the mechanisms of thermoregulation. Second, we discuss recentdevelopments to estimate the »precision« of thermoregulation, and the contribution of distinct be-havioural mechanisms. Finally, we revise available evidence for the existence of evolutionary ad-justments of thermal characteristics in lacertid lizards. Existing studies have mainly dealt withwithin- and among-species differences in thermoregulatory behaviour (selected temperatures) andthermal physiology of adults (optimal temperatures, heating rates). Available data provide onlylimited evidence for clear-cut evolutionary shifts in thermal physiology characteristics along cli-matic gradients.

Keywords: body temperatures, thermoregulation, thermal sensitivity, Lacertidae

Castilla, A. M., Van Damme, R. & Bauwens, D.: Temperatura tijela u prirodi, mehanizmitermoregulacije i evolucija termalnih karakteristika u lacertidnih gu{tera. Nat. Croat., Vol. 8, No.3., 253–274, 1999, Zagreb.

Raspravlja se o tri aspekta termalne biologije lacertidnih gu{tera. Prvo donosimo pregled do-stupnih podataka o tjelesnoj temperaturi u prirodi (Tb), termalnoj osjetljivosti razli~itih funkcija iodabranih temperatura tijela kod razli~itih vrsta lacertidnih gu{tera. Tako|er se ukratko daju infor-macije o mehanizmima termoregulacije. Drugo, raspravlja se o nedavnim poku{ajima procjene»preciznosti« termoregulacije i koji je doprinos odre|enih mehanizama pona{anja. Na kraju se daje

NAT. CROAT. VOL. 8 No 3 253¿274 ZAGREB September 30, 1999

Croatian Natural History Museum, Demetrova 1, Zagreb, Croatia

pregled dostupnih dokaza o postojanju evolucijskih prilagodbi termalnih osobina lacertidnihgu{terica. Postoje}e studije su se uglavnom bavile razlikama u termoregulacijskom pona{anju (od-abrane temperature) unutar jedne i izme|u vi{e vrsta i termalnom fiziologijom adulta (optimalnetemperature, zagrijavanje). Dostupni podaci daju samo ograni~ene dokaze o jasno odre|enim evo-lucijskim pomacima u karakteristikama termalne fiziologije du` klimatskih gradijenata.

Klju~ne rije~i: temperatura tijela, termoregulacija, termalna osjetljivost, Lacertidae

INTRODUCTION

The thermal characteristics of the environment have a pronounced impact on theheat balance and the resulting body temperatures (Tb) of ectotherms (PORTER et al.,1973; PORTER & TRACY, 1983). The Tbs of ectotherms in turn affect the rate at whichbiochemical and physiological processes proceed and thereby influence whole-animal performance functions and hence fitness (HUEY & STEVENSON, 1979; HUEY,1982). Consequently, most reptiles attempt to buffer changes in ambient heat loadsto keep their Tbs at a relatively constant level or, perhaps more realistically, be-tween lower and upper threshold temperatures (BERK & HEATH, 1975; BARBER &CRAWFORD, 1977; HUEY, 1982; VAN BERKUM et al., 1986).

When faced with temporal (i.e., short-term) or geographical (i.e. long-term)variation of the thermal environment, lizards and many other ectotherms exhibittwo types of responses. The first consists of fast-acting thermoregulatory adjust-ments. Lizards regulate their Tb primarily by modifying aspects of their behaviour,although short-term physiological adjustments may also be important (BARTHOLO-

MEW, 1982). Such regulatory behaviours include changing of activity times, selectionof appropriate microhabitats, and postural modifications that alter the rates of heat-ing and cooling (HUEY, 1982; STEVENSON, 1985). These responses are widespreadand well-documented (e.g., HUEY et al., 1977; HUEY, 1982; VAN DAMME et al., 1987;ADOLPH, 1990; BAUWENS et al.,1990, 1996). Because thermoregulatory behaviourshave an immediate effect on Tbs, they are especially efficient in coping with short-term (i.e., daily or seasonal) fluctuations of ambient temperatures. Behavioural ad-justments are also important, at least in part, to cope with permanent differences inenvironmental conditions, such as those faced by populations or species that livealong a climatic gradient (e.g., HERTZ, 1981; HERTZ & HUEY, 1981; HERTZ & NEVO,1981; VAN DAMME et al., 1990). However, the effect of behavioural adjustments onTb is not unlimited but constrained by environmental conditions. In addition, thetime and energy that lizards spend in thermoregulation may curtail those availablefor other activities. Hence, behavioural adjustments are probably not entirely effi-cient in compensating for long-term, geographical differences in ambient condi-tions.

The second type of response consists of evolutionary changes in physiology andbehaviour that increase the time that Tb can be maintained near the level that maxi-mises ecologically important performance capabilities (HUEY & STEVENSON, 1979;HERTZ et al., 1983; HUEY & KINGSOLVER, 1989). These include evolutionary shifts inthe thermal sensitivity of performance functions, changes of the preferred tempera-ture levels and modifications in behavioural or physiological attributes that facili-

254 Castilla, A. M. et al.: Field body temperatures, mechanisms of thermoregulation and evolution ...

tate the attainment of the optimal or preferred temperatures. Although such adjust-ments were once believed to be non-existent (BOGERT, 1949; HERTZ et al., 1983), thereis growing evidence that closely-related lizard taxa exhibit evolutionary differencesin thermal characteristics in relation to variation in ambient heat loads (e.g., HUEY &WEBSTER, 1976; VAN BERKUM, 1986; HUEY & BENNETT, 1987; SINERVO, 1990; BAUWENS

et al., 1995; DÍAZ et al., 1996a).In this paper we summarise current knowledge of several aspects of the thermal

biology of European lacertid lizards. We do not aim to provide a complete over-view of all topics that have received attention by researchers. Rather, we will high-light some aspects that we consider of particular interest to students of lizard ther-mal biology in general and of lacertid lizards in particular. Hence, our owninterests and work unashamedly bias this review. Our specific objectives are three-fold. First, we provide an overview of the available data on the activity Tbs, thethermal sensitivity of various performance functions and selected body tempera-tures in different species. We indicate that information on these different aspects,and on environmental factors, is needed to gain insight into the causes and conse-quences of variation in Tbs. We also briefly summarise information on the mecha-nisms of thermoregulation. Second, we examine to what extent lacertid lizardsregulate their Tb and evaluate the contribution of distinct types of behavioural ad-justments. Specifically, we argue that answering these questions requires the ex-plicit formulation of null hypotheses and a specifically designed research protocol.We also indicate how modifications of this protocol have been used to answer re-lated questions. Third, we revise evidence for the existence of evolutionary shifts ofthermal physiology traits (heating rates, thermal sensitivity profiles) and examinewhether the observed differences parallel variations in environmental characteris-tics.

FIELD, SELECTED AND OPTIMAL TEMPERATURES IN EUROPEANLACERTIDS

Soon after the disclosure by SERGEYEV (1939) and COWLES & BOGERT (1944) thatlizards regulate their Tbs within a surprisingly narrow range, thermal ecology be-came a popular topic in herpetology. Ever since, few field herpetologists have de-parted on their voyages without a quick reading thermometer, and many a lizardcloaca has been uninvitedly probed. At first, studies centered on teiid and iguanidspecies from the deserts and semi-deserts of the United States (BRATTSTROM, 1965),but soon the fashion of »noosing and goosing« lizards blew over to Europe anddata on the thermal biology of lacertid lizards steadily accumulated. A recent (buthasty) scan of the literature revealed nearly 40 studies reporting field body tem-peratures on more than 50 species of Lacertidae (Tab. 1). Comparison and interpre-tation of the results is, however, hampered by the inevitable divergence in scope ofthe different studies. Some have collected data over a complete activity season, oth-ers during a single month and some sampled only during the course of a few days.There is also a strong influence of the levels of activity and catchability of the liz-

Nat. Croat. Vol. 8(3), 1999 255


Tab. 1. Studies on field and selected body temperatures of lacertid lizards

Species Reference

Acanthodactylus boskianus Duvdevani & Borut 1974; Pérez-Mellado 1992,

Acanthodactylus erythrurus Busack 1976; Roman 1982; Carretero & Llorente 1991; Bauwens et al.1995

Acanthodactylus longipes Pérez-Mellado 1992

Acanthodactylus pardalis Duvdevani & Borut 1974

Acanthodactylus schreiberi Duvdevani & Borut 1974

Acanthodactylus scutellatus Duvdevani & Borut 1974; Pérez-Mellado 1992

Algyroides nigropunctatus Arnold 1987

Aporosaura anchietae Brain 1962

Eremias arguta Böhme 1981

Eremias lineo-ocellata Huey et al. 1977

Eremias lugubris Huey et al. 1977

Eremias namaquensis Huey et al. 1977

Eremias pleskii Ushakov & Darevsky 1960 in Cloudsley-Thompson 1971

Eremias spekii Bowker 1984

Eremias strauchii Ushakov & Darevsky 1960 in Cloudsley-Thompson 1971

Gallotia atlantica Márquez et al. 1997

Gallotia caesaris Márquez et al. 1997

Gallotia simonyi Barbadillo 1987; Márquez et al. 1997

Gallotia stehlini Márquez et al. 1997

Ichnotropis squamulosa Huey et al. 1977

Lacerta agilis Liberman & Pokrovskaja 1943; Tertyshnikov 1976; Bauwens et al.1995

Lacerta andreanszkyi Busack 1987

Lacerta bedriagae Bauwens et al. 1990

Lacerta dugesii Crisp et al. 1979

Lacerta graeca Arnold 1987; Maragou et al. 1997

Lacerta horvathi Arnold 1987; De Luca 1991

Lacerta monticola Martinez-Rica 1977; Busack 1978; Pérez-Mellado 1982; Arnold1987; Bauwens et al. 1995

Lacerta mosorensis Arnold 1987

Lacerta oxycephala Arnold 1987

Lacerta schreiberi Salvador & Argüello 1987; Bauwens et al. 1995

Lacerta viridis Arnold 1987

Lacerta vivipara Avery 1976; Patterson & Davies 1978; Clerx & Broers 1983; VanDamme et al. 1986, 1987, 1989; Heulin 1987

Latastia longicaudata Bowker 1984

Meroles cuneirostris Brain 1962

ards: many studies are heavily biased towards records taken during the coolerparts of day. Despite these potential pitfalls, we will attempt to highlight some gen-eralities that emerge from the data.

Average field Tbs for lacertids range between 27 and 40°C, with a median of33.8°C and 50% of all averages falling between 31.9 and 35.5°C (averages for 88populations of 53 species). Most lacertids thus seem to maintain Tbs that are wellabove those of nocturnal lizards (Gekkonidae, Eublepharidae) and lizards from(sub)tropical forests (Chamaeleoninae, Polychrotinae) and are comparable to thoseof (semi-)arid zone lizards (Agaminae, Iguanidae, Tropiduridae, Teiidae, Varanidae,Scincidae).

As data accumulated, it became clear that no single Tb characterises a lizard spe-cies. Within populations, field Tbs of lacertid lizards have been shown to vary withseason (HUEY et al., 1977; ARNOLD, 1987; VAN DAMME et al., 1987; ARGÜELLO & SAL-

VADOR, 1988; JI et al., 1996) and time of day (HUEY et al., 1977; ARGÜELLO & SALVA-

Nat. Croat. Vol. 8(3), 1999 257

Meroles suborbitalis Huey et al. 1977

Mesalina guttulata Pérez-Mellado 1992

Mesalina olivieri Pérez-Mellado 1992

Nucras intertexta Huey et al. 1977

Nucras tesselata Huey et al. 1977

Ophisops elegans Pérez-Mellado et al. 1993

Podarcis atrata Castilla & Bauwens 1991; Bauwens et al. 1995

Podarcis bocagei Pérez-Mellado 1983; Bauwens et al. 1995

Podarcis erhardii Kasapidis et al. 1995

Podarcis hispanica Busack 1978; Pérez-Mellado 1983; Arnold 1987; Carretero &Llorente 1991; Bauwens et al. 1995

Podarcis lilfordi Bauwens et al. 1995

Podarcis melisellensis Arnold 1987

Podarcis milensis Kasapidis et al. 1995

Podarcis milensis Arnold 1987

Podarcis muralis Avery 1978; Arnold 1987; Braña 1991; Bauwens et al. 1995

Podarcis peloponnesiaca Maragou et al. 1997

Podarcis pituyensis Pérez-Mellado & Salvador 1981

Podarcis sicula Avery 1978; Arnold 1987; Van Damme et al. 1990

Podarcis taurica Cruce 1972; Arnold 1987

Podarcis tiliguerta Van Damme et al. 1989

Psammodromus algirus Busack 1978; Roman 1982; Pollo-Mateos & Pérez-Mellado 1987;Carrascal & Díaz 1989; Carretero & Llorente 1991; Bauwens et al.1995; Díaz 1997;

Psammodromus hispanicus Pollo-Mateos & Pérez-Mellado 1989; Bauwens et al. 1995

Takydromus septentrionalis Li et al. 1996

DOR, 1988; VAN DAMME et al., 1990; CASTILLA & BAUWENS, 1991). Body temperaturefluctuations sometimes, but not always, follow variation in environmental tempera-tures to some extent. Mean Tbs in the field may also vary among age classes andsexes (SALVADOR & ARGÜELLO, 1987; CASTILLA & BAUWENS, 1991; CARRASCAL et al.,1992), and, in females, may depend on the reproductive status (VAN DAMME et al.,1987; HEULIN, 1987; TOSINI & AVERY, 1996b). Among populations and species, meanactivity Tbs have been shown to vary with altitude (VAN DAMME et al., 1989, 1990;DÍAZ, 1997) and latitude (ARNOLD, 1987).

Understanding the causes of such variation is not easy and requires additionalinformation on both the animal and its environment. Variation in field Tbs may re-flect both environmental differences and differences in thermal preferences by thelizards. The range of Tbs that a lizard can possibly attain in the field (operative tem-peratures, see further) depends on a number of environmental variables and onseveral morphological and physiological characteristics of the lizard itself. Some ofthe environmental variables (e.g., air and substrate temperature) are known to beimportant, and are often reported. Other variables (e.g., wind speed, radiation) areprobably as important, but are more difficult to measure and therefore remain un-mentioned.

Animal characteristics likely to influence the range of possible Tbs include thelizard’s size, shape, and colour. For instance, juvenile lizards with smaller bodymass and high surface-to-volume ratios heat and cool faster than adults (CARRAS-

CAL et al., 1992; MARTIN et al., 1995). Surprisingly, melanic lacertids do not seem toheat measurably faster than non-melanic lizards (CRISP et al., 1979; TOSINI & AVERY

1993). Some of these »characteristics« may be under control of the lizards or mayhave evolved to meet the needs of the environment. Many species of lacertids alterthe shape of their body to capture more solar radiation (flattening, see further).Heating rates may also be under physiological control; Lacerta viridis increases itsconductance during the sunny parts of the day, and decreases it at the end of theday (RISMILLER & HELDMAIER, 1985, see also further). Some of the interspecificvariation in heating rate seems to be adaptive, with fast heating rates in cool-temperate lizards and slower heating rates in Mediterranean species (DÍAZ et al.,1996a)

In theory, both animal and environmental variables could be measured and fedinto an energy balance equation (PORTER & TRACY, 1983; VAN DAMME et al., 1987) toobtain predictions on the range of attainable Tbs. A much more convenient way isthe use of hollow copper replicas of lizards (see further).

The range of operative temperatures delineates the physically feasible. At theother extreme lies the physiologically ideal. Body temperatures are known to affectmany important whole-animal processes of lacertids (Tab. 2). Physiological per-formance is typically zero below a critical minimum, poor at low body tempera-tures, rises to an optimum (Topt) and then rapidly falls to become zero again at anupper critical temperature. Ideally, a lizard would like to keep its Tb near Topt, or atleast within a range of temperature at which performance is at 80 or 95% of itsmaximum (the 80 and 95 thermal performance breadth, TPB). Several studies havecompared field Tbs of lacertid lizards to thermal sensitivity curves determined in


the field. In most cases, individuals of Podarcis tiliguerta (VAN DAMME et al., 1989),Podarcis atrata (CASTILLA & BAUWENS, 1991), Psammodromus algirus (DIAZ, 1997),Takydromus septentrionalis (JI et al., 1996) and Lacerta vivipara in the field were able torun at more than 80% of their maximal performance, although in the latter species,performance levels were greatly reduced under cloudy and variable weather condi-tions (VAN DAMME et al., 1991).

The use of Topt and TPBs as a yardstick for the »physiologically« ideal is some-what thwarted by both practical and theoretical problems. Practically, determiningthermal sensitivities of whole-animal functions is often laborious. This prevents themeasurement of large numbers of individuals and, as a consequence, little isknown about factors that may cause variation in thermal sensitivity curves. Theo-retically, choosing a relevant function may be difficult. Because of its apparent im-portance for survival, and because of the relative ease with which it can be meas-ured, sprint speed is by far the favourite performance measure taken. But fordifferent animals, and at different times, other functions (e.g. gametogenesis, em-bryonic development, food intake, digestion, growth) may be more important.Choosing the right function becomes especially tricky when different physiologicalfunctions tend to have different thermal sensitivity curves, as has been suggested inlacertids (VAN DAMME et al., 1991; JI et al., 1996).

One way around these practical and theoretical problems is to use body tem-peratures selected (Tsel) in a thermal gradient as a yardstick. The body tempera-tures that lizards adopt in an artificial environment with extremely low costs ofthermoregulation are thought to reflect a behavioural choice that maximises the

Nat. Croat. Vol. 8(3), 1999 259

Tab. 2. Studies of the thermal dependence of various functions in lacertid lizards

Metabolic rate, respiration, ventilation, heart rate

Gelineo & Gelineo 1955; Nielsen 1961; Gelineo 1964; Tromp & Avery 1977; Cragg 1978;Al-Sadoon & Spellerberg 1985; Al-Sadoon 1986, 1987; Al-Sadoon & Abdo 1991; de Vera Porcell& Gonzalez 1986ab;

Foraging efficiency, prey selection, food intake rate, handling time, digestion, growth rate

Avery et al. 1982; Avery 1984; Avery & Mynott 1990; Van Damme et al. 1991; Díaz 1994a; Ji etal. 1996

Locomotion, sprint speed, voluntary speed, gait characteristics, muscle activity

Avery & Bond 1989; Van Damme et al. 1989, 1990a, 1991; Li & Liu 1994; Bauwens et al. 1995; Jiet al. 1996

Chemosensory examination, anti-predatory behaviour

Van Damme et al. 1990b

Gametogenesis, reproductive cycle

Brizzi & Galcano 1969; Fisher 1969; Licht et al. 1969; Brizzi et al. 1976ab; Joly & Saint-Girons1981; d’Uva et al. 1982, 1983; Gavaud 1991

Incubation time, developmental rate, hatchling phenotype

Maderson & Bellairs 1962; Raynaud & Chandola 1969; Oka 1981, Zakharov et al. 1982; Jensen1982; Strijbosch 1988; Rykena 1988; Van Damme et al. 1992; Castilla & Swallow 1996

physiological needs. If different physiological functions have different thermal sen-sitivities, then the median Tsel may at any time represent a compromise that opti-mises all functions jointly, or optimises those functions that are most important atthe given time. The latter possibility seems more likely, since many studies havedemonstrated that Tsel is not the invariant, static, evolutionarily-conservative char-acter it was once believed to be (STEBBINS et al., 1967; HUEY & WEBSTER, 1976; RUI-

BAL & PHILIBOSIAN, 1970; BRADSHAW et al., 1980). In lacertids, Tsel has been shown tovary with season (PATTERSON & DAVIES, 1978; VAN DAMME et al., 1986; RISMILLER &HELDMAIER, 1988), photoperiod (RISMILLER & HELDMAIER, 1982, 1988), time of day(RISMILLER & HELDMAIER, 1982), and may differ between age classes and sexes (PAT-

TERSON & DAVIES 1978; VAN DAMME et al., 1986; CASTILLA & BAUWENS, 1991; MAR-

QUEZ et al., 1997). Nutritional state (BRADSHAW et al., 1980; SIEVERT, 1989), environ-mental moisture (BURY & BALGOOYEN, 1976), and disease (WARWICK, 1991) havebeen reported to affect Tsel in other lizard families.

In some cases, the variation in Tsel can be related to specific physiological func-tions. For instance, the relative high Tsel of adult male Lacerta vivipara in late sum-mer and early spring has been linked tentatively to spermatocyto- and spermio-genesis during these periods; adoption of a low Tsel by females of this species maybe related to the low thermal optimum of the in vitro development of embryos(VAN DAMME et al., 1986). In many other cases, the physiological reasons for the ob-served variation in Tsel remain unclear.

Careful observation of lizards in thermogradients revealed that thermoregulationdoes not revolve around a single body temperature, but rather involves two »set-point« temperatures; an upper setpoint (Tmove, Shade Seeking Tb) at which the liz-ard ceases basking and starts a foraging bout, and a lower setpoint (Tbask, BaskingTb), at which basking is resumed. Either or both setpoints may show intra- and in-terspecific variation (TOSINI & AVERY 1993, 1996B; BELLIURE et al., 1996). The set-point temperatures play an important role in the investigation of the proximatecues that influence thermoregulatory behaviour (TOSINI & AVERY 1993, 1996A,1996B; TOSINI et al., 1995).

Most lacertid lizards will try to move their Tbs into a subset of all possible tem-peratures that is close to the »physiological ideal«. Although some species may becapable of limited physiological adjustments of body temperatures (RISMILLER &HELDMAIER, 1985, GONZALEZ & VERA, 1986), thermoregulation is largely behav-ioural. Lacertids regulate Tb by adjusting activity times, by selecting thermally fa-vourable microhabitats, and by using postural adjustments that alter heat exchangewith the environment (BAUWENS et al., 1996). Restriction of activity times to periodswith suitable weather conditions occurs on a seasonal base (hibernation), as well ason a diel base. Cool temperate species such as Lacerta vivipara and L. agilis (HOUSE

et al., 1980) and montane species such as Lacerta monticola (ARGÜELLO & SALVADOR,1988) and Lacerta bedriagae (BAUWENS et al., 1990) seem to be active throughout theday as long as the conditions are favourable. Bimodal circadian rhythms of activity,with peaks after sunrise and in the afternoon, and a low at noon, have been de-scribed in Mediterranean species such as Psammodromus algirus (CARRASCAL &DÍAZ, 1989) and Podarcis atrata (BAUWENS et al., 1996), and in species from desert ar-


eas such as Acanthodactylus scutellatus, A. boskianus, A. longipes, Meroles olivieri(PÉREZ-MELLADO, 1992) and Eremias lineoocellata (HUEY et al., 1977). However, thefact that fewer individuals are seen during the hottest hours of the day may notmean that lizards are not active; they may be confined to more shady and shelteredplaces, but still remain fully alert and foraging (AVERY, 1993).

The selection of favourable microhabitats usually involves shuttling between hot(usually sunlit) areas and cool (shaded) areas. The frequency and duration of boththese movements and the interspersed periods of stationary basking have beenshown to vary (DÍAZ, 1991; CARRASCAL et al., 1992; BELLIURE et al., 1996). Basking(heliothermy) seems to be the predominant way to increase heat loads in lacertidlizards, although species inhabiting subalpine environments may occasionally ab-sorb some heat from rocks (thigmothermy; e.g., Lacerta monticola, MARTINEZ-RICA,1977; MARTÍN et al., 1995).

Many lacertid lizards employ postural adjustments to optimise heating rateswhile basking. They position themselves on surfaces that face the sun and flattenthe body dorso-ventrally to maximise the incidence of solar radiation on the dorsalpart of the body (AVERY, 1976; VAN DAMME et al., 1987; BAUWENS et al., 1990; CAR-

RASCAL et al., 1992; MARTÍN et al., 1995). Basking postures are most pronounced incool-climate lacertids and less common or even unknown from Mediterranean spe-cies (DÍAZ et al., 1996a).

Although bringing the Tb close to the physiological ideal may seem beneficial,thermoregulation may also be costly, in terms of energy (needed for shuttling) andtime (for shuttling, basking). In addition, thermoregulating lizards may be moreconspicuous to predators. The precision with which lizards will thermoregulate isthought to be a function of both the costs and the benefits of thermoregulation(HUEY & SLATKIN, 1976). As both costs and benefits may vary considerably in timeand space (see above), it is not surprising to see that the degree of thermoregula-tion may do the same (HEULIN, 1987; VAN DAMME et al., 1987; 1989; SALVADOR &ARGÜELLO, 1987; CARRASCAL et al., 1992; JI et al., 1996; DÍAZ, 1997). However, themeasurement of the accuracy and precision of thermoregulation has long beenclouded by some methodological shortcomings.

THE ACCURACY AND MECHANISMS OF BEHAVIOURALTHERMOREGULATION

Behavioural adjustments are the primary means by which lizards buffer fluctua-tions in ambient heat loads to maintain their Tbs within the range that is conduciveto optimal performance. Nevertheless, environmental conditions exert physical lim-its to the Tbs that can be achieved and biotic considerations, such as the diversionof available time and energy to distinct demands, may curtail the time devoted tobehavioural thermoregulation. Hence, a question that has for a long time directedfield studies of thermal biology is: How carefully do lizards thermoregulate? Al-though this question seems simple and straightforward, only recently have the con-

Nat. Croat. Vol. 8(3), 1999 261

ceptual and methodological advances been made that make it possible to providean adequate answer (HERTZ et al., 1993).

The notion of »thermoregulation« implies that organisms actively use behaviouralor physiological adjustments to (i) divert their Tbs from those that would result fromthe passive exchange of heat with the environment (i.e., in the absence of regulatoryprocesses), and (ii) maintain Tbs within a preference zone (i.e., the »set-point« range).Indices that have traditionally been used as measures of temperature regulation donot, or do only partially, capture this concept of thermoregulation (see HERTZ et al.,1993 for a detailed account). For instance, the variance in Tb does not account forvariation in ambient conditions, nor does it make any reference to the set-point range(VAN DAMME et al., 1987, 1989; HERTZ et al., 1993). The slope of the regression of Tbon air temperature (HUEY & SLATKIN, 1976) is also inappropriate because it ignoresthe set-point range, and because air temperature provides a very incomplete pictureof the thermal heat loads that a lizard experiences (PORTER et al., 1973; PORTER &TRACY, 1983; VAN DAMME et al., 1987; DREISIG, 1984; HERTZ et al., 1993).

A comprehensive analysis that considers the different facets of temperature regu-lation requires at least three kinds of data (HERTZ et al., 1993). First, one must docu-ment the Tbs of a representative sample of field active animals. Second, one must in-dependently identify the »set point« range or, alternatively, the range of selectedtemperatures, as an estimate of the target Tbs that ectotherms maintain in the absenceof environmental constraints on temperature regulation (HEATH, 1965; LICHT et al.,1966). Third, one requires the distribution of operative temperatures (Tes) at differenttimes and in all available microhabitats. These Tes can be measured with hollow-bodied copper models that mimic the size, shape and radiative properties of lizardsand integrate the effect of various biophysical factors (e.g., air temperature, solar ra-diation, wind) that affect a lizard's heat balance (BAKKEN, 1992; HERTZ, 1992). Hence,the Tes estimate the equilibrium Tbs of non-thermoregulating animals. When modelsare randomly placed in the distinct available microhabitats, appropriate null hy-potheses of »no thermoregulation« can be formulated. This is a prerequisite to dem-onstrate unequivocally that organisms do regulate their Tb (HEATH, 1964; HUEY et al.,1977; GRANT & DUNHAM, 1988; ADOLPH, 1990; HERTZ, 1992; DÍAZ, 1994b).

We used this protocol to study temperature regulation by the lizard Podarcisatrata during sunny days in early autumn (BAUWENS et al., 1996). Throughout itsdaily activity period, this lizard maintains remarkably constant Tbs within, or veryclose to, the range of selected temperatures. This indicates that this population ther-moregulates with high accuracy. In addition, the activity Tbs deviated clearly fromthe Tes, especially during early morning and late afternoon, when Tbs were gener-ally higher, and during the middle portion of the day, when Tbs were often lowerthan the Tes. The differences between the actual Tbs and the Tes, which estimate thebody temperatures of non-thermoregulating lizards, must be attributed to the ef-fects of thermoregulatory behaviour, and show that P. atrata thermoregulates veryeffectively.

We used similar methods to study seasonal variation in temperature regulationin Lacerta vivipara (VAN DAMME et al., 1987). The Tbs of free-ranging lizards variedseasonally, being noticeably lower at the onset of the activity period (March-April).


In early spring, Tbs were considerably below the range of selected temperatures,whereas during other months of the year lizards maintained Tbs close to the se-lected range. Estimates of »maximal operative temperatures« demonstrate that en-vironmental conditions during the cooler months actually prevent the lizardsattaining Tbs within the selected range. Thus, the reduced accuracy of thermoregu-lation in early spring is an inevitable consequence of restrictions imposed by thethermal environment. Moreover, lizards maintained their Tbs close to the maximalTes, in other words, as high as was physically possible. Hence, lizards regulatedtheir Tbs at the maximal possible level.

Although similar studies for other species would be highly welcome, these ex-amples reinforce our general impression that European lacertid lizards can be con-sidered as »accurate« and »efficient« thermoregulators. They maintain their Tbsclose to the selected range, at least when ambient conditions allow them to do so,and their Tbs differ clearly from those that would be attained in the absence ofregulatory adjustments. However, the research protocol outlined above does notidentify the behaviours by which lizards thermoregulate.

It is generally acknowledged that the primary mechanisms of behavioural tem-perature regulation include the restriction of activity times, the selection of ther-mally appropriate microhabitats, and postural adjustments that alter rates of heatexchange (e.g., AVERY, 1976; HUEY et al., 1977; HERTZ & HUEY, 1981; HUEY, 1982).AVERY (1993) advocated the performance of more detailed behavioural observationsto elucidate the contribution of distinct behaviours to a regulated Tb. A largenumber of studies on European lacertids use this approach, at least to some extent(e.g., AVERY 1976, 1978, 1993; VAN DAMME et al., 1987, 1989; BAUWENS et al., 1990;CASTILLA & BAUWENS, 1991; DÍAZ, 1991, 1992, 1994; DÍAZ et al., 1996b). However, ob-servations of behaviours can only provide indirect evidence on their pertinence forthermoregulation. For instance, the mere observation that lizards do not use micro-habitats randomly may suggest that microhabitat selection is a mechanism of ther-moregulation, although it may equally well reflect non-random distribution offood, predators or conspecifics.

We recently used a different approach to evaluate the relative contributions ofseveral behavioural mechanisms (activity times, use of microhabitats and sun-shadepatches, basking, and shuttling) to thermoregulation in a population of Podarcisatrata (BAUWENS et al., 1996). To assess the contribution of selection of microsites(combinations of structural microhabitats and sun/shade patches), we combined re-sults from direct behavioural observations with information on the Tes in differentmicrosites at different times of day. Observations indicated that, at different timesof day, lizards did not use microsites in proportion to their availability. To what ex-tent is this nonrandom pattern induced by thermoregulatory considerations?

One extreme strategy would be that lizards restrict activity to thermally favour-able microsites, that is, to sites where Te is within the selected temperature range.We can formalise this »only thermoregulation« hypothesis by identifying, using theTe data obtained with copper models, those microsites that are thermally favour-able at different times of day. Comparison of the actual use of microsites by the liz-ards with the predicted pattern indicates that P. atrata does not adopt this extremestrategy. Thus, lizards did not restrict their activities to thermally favourable sites,

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such that thermoregulatory considerations are not the sole determinants of micro-site selection by the lizards.

What are the thermal consequences of the observed pattern of microsite selec-tion? We can estimate this by calculating a weighted Te-distribution, with theweighing factors proportional to the actual microsite by the lizards. This distribu-tion in fact estimates the expected Tbs of hypothetical lizards that use microsites inthe same way as real lizards do, but that do not exhibit any other form of thermo-regulatory behaviour. The Tes associated with the lizards' use of specific micrositeswere on average ca 2 °C closer to the selected temperature range than were the ran-domly available Tes. In other words, microsite selection alters the heat loads towhich lizards are exposed. They select relatively warm sites when it is cool, andprefer cooler sites during the warmer hours. The thermal consequences of micrositeselection were most apparent during the early morning and late afternoon hours(BAUWENS et al., 1996).

In the former paragraphs we described how measurements of Tes were used ex-plicitly to test hypotheses about thermoregulation and the thermal consequences ofparticular aspects of behaviour. The conclusions that lizards thermoregulate effec-tively and that microhabitat selection does contribute to temperature regulation arenot surprising, and coincide with common expectations. Hence, some may findthese findings »obvious« and the research procedures unnecessarily cumbersome. Itshould, however, be recognized that progress in science is too often hampered bythe acceptance of seemingly long established »facts« that have never, or only veryrarely, been tested.

We also note that Te measurements can be used to estimate and compare the ther-mal quality of different macrohabitats. This forms a basis to formulate testable hy-potheses on the putative relation between the thermal suitability of habitats anddemographic parameters. DÍAZ (1997) gives an excellent example of this application.

EVOLUTION OF THERMAL PHYSIOLOGY CHARACTERISTICS

Thermoregulatory behaviour is the primary means by which lizards buffer fluc-tuations of the thermal environment. However, abiotic conditions may temporarilyimpede lizards from achieving Tbs within the selected range and this may be asso-ciated with a reduction of their performance capacities. When such restrictions ac-quire a permanent character, for instance when climatic conditions change, naturalselection should favour a shift in physiological characteristics, to restore perform-ance to its maximal levels (HERTZ et al., 1983; HUEY & BENNETT, 1987; HUEY & KING-

SOLVER, 1989). Here we summarise results of comparative studies that examinedwhether physiological adjustments to climatic conditions have evolved in Europeanlacertid lizards.

Interspecific variation in heating rates

Many species of lacertid lizards spend much time increasing their Tb by »bask-ing« (e.g., AVERY, 1976; VAN DAMME et al., 1987, 1989; BAUWENS et al., 1996). This re-


duces the time available for other activities. It seems reasonable to assume that liz-ards will attempt to minimise the time spent heating, to prolong the time that Tbcan be maintained within the selected range. Because lizards that inhabit cool cli-mate zones require more time to warm to their selected temperature, we expectthat they exhibit compensatory physiological (and behavioural) adjustments thatincrease the rate of heat gain. Hence, the hypothesis of evolutionary adjustments ofthermal physiology in relation to climatic conditions predicts that heating rates willbe fastest in species that inhabit the coolest environments. This idea was recentlyexamined by DÍAZ et al. (1996a).

These authors compared heating rates, measured under standardised laboratoryconditions, of eight species of lacertids that live in diverging climate zones. Phylo-genetically based analyses of covariance show that species with a northern/mon-tane distribution warm at a faster mass-specific rate than lizards that inhabit asouthern (Mediterranean) climate area. Correlational analyses, using phylogeneti-cally independent contrasts, confirm that continuous among-species variation inmass-specific heating rates is negatively related to clinal differences in ambienttemperatures in the lizards' habitats. In other words, species that inhabit relativelycool areas heat faster than similarly sized lizards from warmer areas. This is exactlythe pattern that is predicted by the hypothesis of evolutionary adjustments of ther-mal physiology in relation to climatic conditions. Hence, these results are consid-ered strong evidence for the existence of adaptive adjustments of heating rates toclimatic conditions within this clade of lacertid lizards (DÍAZ et al., 1996a).

Intra- and interspecific variation in the thermal optimum of sprint speed

Sprint speed, which is considered an ecologically important whole-animal per-formance trait (GARLAND & LOSOS, 1994), is highly dependent on the lizards' Tb. Toachieve maximal sprinting speed, lizards should maintain their Tb close to thephysiological optimum temperature for sprinting. Species or populations that livein diverging climates, and that maintain different activity Tbs, are therefore ex-pected to exhibit parallel differences in the optimal temperature for sprint speed.This hypothesis was examined at both the intra- and interspecific level.

VAN DAMME et al. (1989, 1990) compared two populations of both Lacerta viviparaand Podarcis tiliguerta living at different altitudes (sea level and mountain). In bothcases the ambient temperatures and the Tbs maintained during activity were sig-nificantly lower at the mountain sites. However, in neither of the two species didthe populations differ in the optimal temperature for sprinting. Thus, populationsof these species that live in diverging climate conditions have not evolved paralleldifferences in the thermal sensitivity of sprinting speed. Similar findings have beenreported in an agamid (HERTZ et al., 1983) and a phrynosomatid lizard (CROWLEY,1985). In both cases, differences in ambient conditions were associated with parallelvariation in activity Tbs, but not with among-population differences in the optimaltemperature for sprint speed.

BAUWENS et al. (1995) studied the thermal sensitivity of sprinting speed in 13species of European lacertid lizards that live along a climatic gradient. There wereclear-cut among-species differences in the optimal temperature for sprinting. Thus,different species have evolved different optimal temperatures for running speed.

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However, the critical question is whether the variation in optimal temperatures isrelated to differences in the thermal environment (i.e., ambient temperatures). Thedata do not provide evidence for the existence of a tight, positive relation. Hence,these results do not support the hypothesis of adaptation of the thermal sensitivityof sprinting to ambient conditions. At the same time, however, they do not falsifythis hypothesis.

The hypothesis of adaptation adjustments of the thermal physiology predicts arelationship with ambient temperatures only when variation in environmental con-ditions translates directly into differences in activity Tbs. Indeed, it is the Tbs main-tained during activity that affect performance capacities, not the ambient tempera-tures alone. Through the extensive use of short-term behavioural adjustments, theTbs of lacertid lizards deviate notably from the ambient temperatures. Hence, spe-cies that live in different climates may maintain identical activity Tbs, because theydisplay different thermoregulatory behaviours or because they invest differentamounts of time in behavioural temperature regulation. Thus, a more stringent testof the hypothesis would be to search for a putative relationship between the opti-mal temperature and the Tbs maintained by active animals. Regretfully, the lowlevel of standardisation among published data of field Tbs in the lacertids impedesa thorough test of this prediction.

VAN BERKUM (1986) provided support for this hypothesis in a group of Anolis liz-ards that live along an altitudinal gradient. She found, as predicted, a clear positiverelationship between the optimal temperature of sprint speed and the activity Tbs ex-perienced by different species in nature. It is worth noting that the Anolis speciesstudied have far more restricted thermoregulatory abilities, and hence exhibit muchlarger among-species differences in Tbs than the European lacertid lizards.

In addition, BAUWENS et al. (1995) report, within a clade of lacertids, a positiveevolutionary correlation between the optimal temperature for sprinting and the me-dian selected temperature. This result gives evidence that the evolution of the ther-mal sensitivity of sprint speed has proceeded in concert with the evolution of theset-point range of Tbs that lizards attempt to achieve during activity. This resultsupports the hypothesis of adaptive adjustments of the thermal sensitivity to theactivity Tbs, but only if we assume that the field Tbs match the selected tempera-tures in all species. Available data do not allow us to test this assumption. Somestudies have shown that, during some periods of the day or year, ambient condi-tions prevent lizards achieving the selected temperatures in the field (VAN DAMME

et al., 1987, 1989, 1990). However, it is at present unclear whether this occurs in onlysome populations or species, or is a more general phenomenon.

ACKNOWLEDGEMENTS

During preparation of the manuscript we were illuminated by the harmoniousphenotypes of Penélope Cruz, Robert Redford and Inés Sastre. AMC is supportedby a contract of the Spanish CSIC; RVD is a senior research assistant of the FWO –Flanders.

Received August 11, 1998


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S U M M A R Y

Field body temperatures, mechanisms of thermoregulation andevolution of thermal characteristics in lacertid lizards

A. M. Castilla, R. Van Damme & D. Bauwens

We discuss three aspects of the thermal biology of lacertid lizards. First, we pro-vide an overview of the available data on field body temperatures (Tb), the thermalsensitivity of various performance functions and selected body temperatures in dif-ferent species of lacertid lizards. We also briefly summarise information on themechanisms of thermoregulation. Second, we discuss recent developments to esti-mate the »precision« of thermoregulation, and the contribution of distinct behav-ioural mechanisms. This requires predictions of the Tbs of non-thermoregulatinglizards. Such null hypotheses are provided by measurements of operative tempera-tures using copper models of lizards. Studies that used this protocol indicate thatlacertids thermoregulate with high »precision«, »accuracy« and »effectiveness«. Themain behavioural mechanisms are the restriction of activity times, microhabitatchoice, shuttling between microhabitats and overt basking. We show that the con-tributions of each of these adjustments to temperature regulation can be evaluatedby the formulation of specific null-hypotheses, comparison with distributions of Tband direct behavioural observations. Finally, we revise available evidence for theexistence of evolutionary adjustments of thermal characteristics in lacertid lizards.Existing studies have mainly dealt with within- and among-species differences inthermoregulatory behaviour (selected temperatures) and thermal physiology ofadults (optimal temperatures, heating rates). Available data provide only limitedevidence for clear-cut evolutionary shifts in thermal physiology characteristicsalong climatic gradients.

Nat. Croat. Vol. 8(3), 1999 273

S A @ E TA K

Temperatura tijela u prirodi, mehanizmi termoregulacije i evolucijatermalnih karakteristika u lacertidnih gu{tera

A. M. Castilla, R. Van Damme & D. Bauwens

Raspravlja se o tri aspekta termalne biologije lacertidnih gu{tera. Prvo donosimopregled dostupnih podataka o tjelesnoj temperaturi u prirodi (Tb), termalnoj osjetl-jivosti razli~itih funkcija i odabranih temperatura tijela kod razli~itih vrsta lacertid-nih gu{tera. Tako|er se ukratko daju informacije o mehanizmima termoregulacije.Drugo, raspravlja se o nedavnim poku{ajima procjene »preciznosti« termoregulacijei doprinosu odre|enih mehanizama pona{anja. To zahtijeva predvi|anja Tb-a ne-termoreguliraju}ih gu{tera. Takve nul-hipoteze omogu}avaju mjerenja operativnihtemperatura kori{tenjem bakrenih modela gu{tera. Studije u kojima su kori{tenitakvi protokoli ukazuju na to da lacertidni gu{teri termoreguliraju s visokom »pre-cizno{}u«, »to~no{}u« i »efektivno{}u«. Glavni mehanizmi pona{anja su ograni~enjevremena aktivnosti, izbor mikrostani{ta, izmjene izme|u mikrostani{ta i o~itog»sun~anja«. Pokazali smo da se doprinosi svake od ovih prilagodbi na regulacijutemperature mogu procijeniti formuliranjem specifi~nih nul-hipoteza, usporedboms raspodjelom Tb i izravnim opa`anjem pona{anja. Na kraju se daje pregled do-stupnih dokaza o postojanju evolucijskih prilagodbi termalnih osobina lacertidnihgu{terica. Postoje}e studije su se uglavnom bavile razlikama u termoregulacijskompona{anju (odabrane temperature) unutar jedne i izme|u vi{e vrsta i termalnomfiziologijom adulta (optimalne temperature, zagrijavanje). Dostupni podaci daju sa-mo ograni~ene dokaze o jasno odre|enim evolucijskim pomacima u karakteristi-kama termalne fiziologije du` klimatskih gradijenata.


implementing a regulatory budget: estimating the mandated private

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